Metabolome phenotyping of inorganic carbon limitation in cells of the wild type and photorespiratory mutants of the cyanobacterium Synechocystis sp. strain PCC 6803.
The amount of inorganic carbon represents one of the main environmental factors determining productivity of photoautotrophic organisms. Using the model cyanobacterium Synechocystis sp. PCC 6803, we performed a first metabolome study with cyanobacterial cells shifted from high CO(2) (5% in air) into conditions of low CO(2) (LC; ambient air with 0.035% CO(2)). Using gas chromatography-mass spectrometry, 74 metabolites were reproducibly identified under different growth conditions. Shifting wild-type cells into LC conditions resulted in a global metabolic reprogramming and involved increases of, for example, 2-oxoglutarate (2OG) and phosphoenolpyruvate, and reductions of, for example, sucrose and fructose-1,6-bisphosphate. A decrease in Calvin-Benson cycle activity and increased usage of associated carbon cycling routes, including photorespiratory metabolism, was indicated by synergistic accumulation of the fumarate, malate, and 2-phosphoglycolate pools and a transient increase of 3-phosphoglycerate. The unexpected accumulation of 2OG with a concomitant decrease of glutamine pointed toward reduced nitrogen availability when cells are confronted with LC. Despite the increase in 2OG and low amino acid pools, we found a complete dephosphorylation of the PII regulatory protein at LC characteristic for nitrogen-replete conditions. Moreover, mutants with defined blocks in the photorespiratory metabolism leading to the accumulation of glycolate and glycine, respectively, exhibited features of LC-treated wild-type cells such as the changed 2OG to glutamine ratio and PII phosphorylation state already under high CO(2) conditions. Thus, metabolome profiling demonstrated that acclimation to LC involves coordinated changes of carbon and interacting nitrogen metabolism. We hypothesize that Synechocystis has a temporal lag of acclimating carbon versus nitrogen metabolism with carbon leading.
Eisenhut
Marion
M
Universität Rostock, Institut für Biowissenschaften, Pflanzenphysiologie, 18051 Rostock, Germany.
Huege
Jan
J
Schwarz
Doreen
D
Bauwe
Hermann
H
Kopka
Joachim
J
Hagemann
Martin
M
D000064:Acclimatization / Q000235:genetics; D001431:Bacteriological Techniques; D002244:Carbon / Q000378:metabolism*; D002245:Carbon Dioxide / Q000378:metabolism; D020869:Gene Expression Profiling; D006016:Glycolates / Q000378:metabolism; D009154:Mutation; D009584:Nitrogen / Q000378:metabolism; D051922:PII Nitrogen Regulatory Proteins / Q000378:metabolism; D010641:Phenotype; D010766:Phosphorylation; D052817:Phototrophic Processes / Q000235:genetics; D046939:Synechocystis / Q000235:genetics / Q000378:metabolism*
D006016:Glycolates; D051922:PII Nitrogen Regulatory Proteins; D002245:Carbon Dioxide; D002244:Carbon; C013193:phosphoglycolate; D009584:Nitrogen